Evolution of the facial musculature in basal ray-finned fishes

Background

The facial musculature is a remarkable anatomical complex involved in vital activities of fishes, such as food capture and gill ventilation. The evolution of the facial muscles is largely unknown in most major fish lineages, such as the Actinopterygii. This megadiverse group includes all ray-finned fishes and comprises approximately half of the living vertebrate species. The Polypteriformes, Acipenseriformes, Lepisosteiformes, Amiiformes, Elopiformes, and Hiodontiformes occupy basal positions in the actinopterygian phylogeny and a comparative study of their facial musculature is crucial for understanding the cranial evolution of bony fishes (Osteichthyes) as a whole.

Results

The facial musculature of basal actinopterygians is revised, redescribed, and analyzed under an evolutionary perspective. We identified twenty main muscle components ontogenetically and evolutionarily derived from three primordial muscles. Homologies of these components are clarified and serve as basis for the proposition of a standardized and unifying myological terminology for all ray-finned fishes. The evolutionary changes in the facial musculature are optimized on the osteichthyan tree and several new synapomorphies are identified for its largest clades, including the Actinopterygii, Neopterygii, and Teleostei. Myological data alone ambiguously support the monophyly of the Holostei. A newly identified specialization constitutes the first unequivocal morphological synapomorphy for the Elopiformes. The myological survey additionally allowed a reinterpretation of the homologies of ossifications in the upper jaw of acipenseriforms.

Conclusions

The facial musculature proved to be extremely informative for the higher-level phylogeny of bony fishes. These muscles have undergone remarkable changes during the early radiation of ray-finned fishes, with significant implications for the knowledge of the musculoskeletal evolution of both derived actinopterygians and lobe-finned fishes (Sarcopterygii).

     

Interrelationships of lower actinopterygian fishes

The lower actinopterygian fishes are classified using dermal skull roof pattern, in particular the various configurations displayed by the bones on the otic branch of the infraorbital canal (dermosphenotic, intertemporal-supratemporal/dermopterotic). Where possible these patterns are related to the sequential acquisition of derived features, and the resulting cladogram represents a synthesis of dermal bone pattern and endochondral and dermal skeletal characters. We have proposed 27 terminal groups which we tentatively regard as monophyletic and have concluded that Polypterus is the most primitive living taxon, that the Chondrostei is the sister-group of Saurichthys and Luganoia the most derived stem-group neopterygian.     

Patterns of genome size diversity in the ray-finned fishes

The ray-finned fishes make up about half of all vertebrate diversity and are by far the best represented group in the Animal Genome Size Database. However, they have traditionally been the least well investigated among vertebrates in terms of patterns and consequences of genome size diversity. This article synthesizes and expands upon existing information about genome size diversity in ray-finned fishes. Specifically, compiled data from the Animal Genome Size Database and FishBase are used to examine the potential patterns of interspecific genome size variability according to ecology, environment, morphology, growth, physiology, reproduction, longevity, and taxonomic diversity. Polyploidy and haploid genome sizes are considered separately, revealing differences in their respective consequences. This represents the most comprehensive summary of fish genome size diversity presented to date, and highlights areas of particular interest to investigate as more data become available.

The transition in hemoglobin proton-binding characteristics within the basal actinopterygian fishes

Carbon dioxide (CO₂) transport in the blood of fishes is aided by the proton-binding properties of hemoglobin (Hb) through either a high-intrinsic buffer value and small oxylabile proton binding (Haldane effect), or a low buffer value and large Haldane effect. Primitive species, such as elasmobranchs and sarcopterygians have been shown to rely on the former, while derived species, such as teleosts rely on the latter. Both strategies are effective in the transport of CO₂ in the blood. However, there is a paucity of information on the nature of the transition between these two strategies that appears to occur within the intermediate group of fishes, the basal actinopterygians. The objective of the present study was to simultaneously assess the intrinsic Hb buffer values and Haldane effects of species within the basal actinopterygian lineage to characterize the transition in Hb-proton-binding strategy seen among the fishes. Expressed in order of most basal to most derived, the species investigated included American paddlefish (Polyodon spathula), white sturgeon (Acipenser transmontanus), spotted gar (Lepisosteus oculatus), alligator gar (Atractosteus spatula), bowfin (Amia calva), and mooneye (Hiodon tergisus). Hemolysates from these species were prepared and Hb titrations (under oxygenated and deoxygenated conditions) were performed in both the presence and absence of saturating levels of organic phosphates (GTP). The findings suggest that the nature of the Hb-proton-binding transition may have been punctuated rather than gradual, with the Hb buffer value decreasing and the Haldane effect increasing significantly in bowfin from fairly steady ancestral levels in the four more basal species. This change is coupled with the initial appearance of the choroid rete, as well as an increase in the magnitude and onset pH of the Root effect in bowfin, suggesting that the change in Hb-proton-binding strategy may be associated with the evolution of enhanced O₂ delivery to the eye and an in vivo operational Root effect.     

Tracing the genetic footprints of vertebrate landing in non-teleost ray-finned fishes

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Ontogeny and phylogeny of tooth attachment modes in actinopterygian fishes

There are four major tooth attachment modes in actinopterygians. Type 1 mode is characterized by complete ankylosis of the tooth to the attachment bone; it is the primitive attachment mode for actinopterygians. In Type 2 mode there is a ring of collagen between the tooth base and the bone. In Type 3 mode mineralization extends near or to the bone at the anterior tooth border, and there is a relatively large collagen area on the posterior surface of the tooth; Type 3 teeth are hinged with an anterior axis of rotation. Type 4 teeth also have a relatively large posterior collagen area, but there is no collagenous connection between the anterior basal tooth border and the attachment bone; Type 4 teeth are hinged, with a posterior axis of rotation. Types 2, 3, and 4 attachment modes appear to result from retardation of mineralization and resemble, with some modifications, ontogenetic stages in the development of Type 1 mode; they are considered to be paedomorphic features. Attachment modes 2, 3, and 4 are each associated with a major evolutionary lineage within the Teleostei. The degree to which paedomorphosis has been a factor in teleostean evolution is discussed.     

Sex chromosomes and male ornaments: a comparative evaluation in ray-finned fishes

Theory predicts that the mechanism of genetic sex determination can substantially influence the evolution of sexually selected traits. For example, female heterogamety (ZZ/ZW) can favour the evolution of extreme male traits under Fisher's runaway model of sexual selection. We empirically test whether the genetic system of sex determination has played a role in the evolution of exaggerated male ornaments in actinopterygiian fishes, a clade in which both female-heterogametic and male-heterogametic systems of sex determination have evolved multiple times. Using comparative methods both uncorrected and corrected for phylogenetic non-independence, we detected no significant correlation between sex-chromosome systems and sexually selected traits in males. Results suggest that sex-determination mechanism is at best a relatively minor factor affecting the outcomes of sexual selection in ray-finned fishes.     

Mating preferences, sexual selection and patterns of cladogenesis in ray-finned fishes

Evolutionary theory predicts that sexual selection may increase taxonomic diversity when emergent mating preferences result in reproductive isolation and therefore speciation. This theory has been invoked to explain patterns of diversity in ray-finned fishes (most notably in the cichlids), but the theory has not been tested comparatively in fish. Additionally, several other unrelated factors have been identified as promoters of cladogenesis, so it is unclear how important sexual selection might be in diversification. Using sister-clade analysis, I tested the relationship between the presence of sexually selected traits and taxonomic diversification in actinopterygiian fishes, a large clade that shows substantial diversity in mating preferences and related sexually selected traits. In all identified sister-families that differed with regard to the proportion of species manifesting sexually selected traits, sexual selection was correlated with increased diversification, and this association was significant across all sister clades (P=0.02). This suggests that sexual selection, when present, is a substantial driver of diversification in the ray-finned fishes, and lends further empirical support to the theoretical link between mating preferences and accelerated cladogenesis.     

Evolution of dimorphisms of the proteasome subunit beta type 8 gene (PSMB8) in basal ray-finned fish

The proteasome subunit beta type 8 (PSMB8) gene encodes a catalytic subunit of immunoproteasome that plays a central role in the processing of antigenic peptides presented by major histocompatibility complex class I molecules. The A- and F-type alleles defined by the 31st amino acid residue determining cleaving specificity have been identified from ray-finned fish, amphibia, and reptiles. These two types show extremely long-term trans-species polymorphism in Polypteriformes, Cypriniformes, and Salmoniformes, suggesting the presence of very ancient lineages termed A and F. To elucidate the evolution of the PSMB8 dimorphism in basal ray-finned fish, we analyzed Pantodon buchholzi (Osteoglossiformes), seven species of Anguilliformes, and Hypomesus nipponensis (Osmeriformes). Both A and F lineage sequences were identified from P. buchholzi and H. nipponensis, confirming that these two lineages have been conserved by basal ray-finned fish. However, both the A- and F-type alleles found in Anguilliformes species belonged to the F lineage irrespective of their types. This apparently suggests that the A lineage was lost in the common ancestor of Anguilliformes, and recovery of the A type within the F lineage occurred in Anguilliformes. The apparent loss of the F lineage and recovery of the F type within the A lineage have already been reported from tetrapods and higher teleosts. However, this is the first report on the reverse situation and reveals the dynamic evolution of the PSMB8 dimorphism.     

The organization of the octavolateralis area in actinopterygian fishes: A new interpretation

The octavolateralis area of actinopterygian fishes can be subdivided into a dorsal lateralis area composed of first-order lateral line nuclei, and a ventral octavus area composed of nuclei receiving first-order input from the eighth nerve. Three patterns of organization of the lateralis area are recognized in the present study. The organization of this area in polypteriforms and chondrosteans is similar to that in chondrichthyans. On the basis of recent studies in chondrichthyans (McCready and Boord, '76; Boord and Campbell, '77; Bodznick and Northcutt, '80), it is hypothesized that this pattern reflects the subdivision of the lateral line system into mechanoreceptive and electroreceptive portions. As petromyzontid agnathans also share this pattern of organization, it is hypothesized that they are elecroreceptive. The lateralis area of holosteans and nonelectroreceptive teleosts exhibits a second organizational pattern that is hypothesized to reflect the loss of the electroreceptive portion of the lateral line system; it is suggested that electroreception was lost sometime between the chondrostean and teleostean radiations. Each group of electroreceptive teleosts is believed to have evolved electroreception independently (Bullock, '74), a situation that is reflected centrally by a third organizational pattern within the lateralis area, which is distinctly different from that of early radiations of electroreceptive fishes. The octavus area of actinopterygians exhibits two patterns of organization–that of polypteriforms, chondrosteans, and holosteans, and that of teleosts. The functional significance of these patterns has yet to be elucidated.     

Optimal data partitioning and a test case for ray-finned fishes (Actinopterygii) based on ten nuclear loci

Data partitioning, the combined phylogenetic analysis of homogeneous blocks of data, is a common strategy used to accommodate heterogeneities in complex multilocus data sets. Variation in evolutionary rates and substitution patterns among sites are typically addressed by partitioning data by gene, codon position, or both. Excessive partitioning of the data, however, could lead to overparameterization; therefore, it seems critical to define the minimum numbers of partitions necessary to improve the overall fit of the model. We propose a new method, based on cluster analysis, to find an optimal partitioning strategy for multilocus protein-coding data sets. A heuristic exploration of alternative partitioning schemes, based on Bayesian and maximum likelihood (ML) criteria, is shown here to produce an optimal number of partitions. We tested this method using sequence data of 10 nuclear genes collected from 52 ray-finned fish (Actinopterygii) and four tetrapods. The concatenated sequences included 7995 nucleotide sites maximally split into 30 partitions defined a priori based on gene and codon position. Our results show that a model based on only 10 partitions defined by cluster analysis performed better than partitioning by both gene and codon position. Alternative data partitioning schemes also are shown to affect the topologies resulting from phylogenetic analysis, especially when Bayesian methods are used, suggesting that overpartitioning may be of major concern. The phylogenetic relationships among the major clades of ray-finned fish were assessed using the best data-partitioning schemes under ML and Bayesian methods. Some significant results include the monophyly of "Holostei" (Amia and Lepisosteus), the sister-group relationships between (1) esociforms and salmoniforms and (2) osmeriforms and stomiiforms, the polyphyly of Perciformes, and a close relationship of cichlids and atherinomorphs.     

The nucleotypic effects of cellular DNA content in cartilaginous and ray-finned fishes.

Cytological and organismal characteristics associated with cellular DNA content underpin most adaptionist interpretations of genome size variation. Since fishes are the only group of vertebrate for which relationships between genome size and key cellular parameters are uncertain, the cytological correlates of genome size were examined in this group. The cell and nuclear areas of erythrocytes showed a highly significant positive correlation with each other and with genome size across 22 cartilaginous and 201 ray-finned fishes. Regressions remained significant at all taxonomic levels, as well as among different fish lineages. However, the results revealed that cartilaginous fishes possess higher cytogenomic ratios than ray-finned fishes, as do cold-water fishes relative to their warm-water counterparts. Increases in genome size owing to ploidy shifts were found to influence cell and nucleus size in an immediate and causative manner, an effect that persists in ancient polyploid lineages. These correlations with cytological parameters known to have important influences on organismal phenotypes support an adaptive interpretation for genome size variation in fishes.     

A Middle Triassic thoracopterid from China highlights the evolutionary origin of overwater gliding in early ray-finned fishes

Gliding adaptations in thoracopterid flying fishes represent a remarkable case of convergent evolution of overwater gliding strategy with modern exocoetid flying fishes, but the evolutionary origin of this strategy was poorly known in the thoracopterids because of lack of transitional forms. Until recently, all thoracopterids, from the Late Triassic of Austria and Italy and the Middle Triassic of South China, were highly specialized ‘four-winged’ gliders in having wing-like paired fins and an asymmetrical caudal fin with the lower caudal lobe notably larger than the upper lobe. Here, we show that the new genus Wushaichthys and the previously alleged ‘peltopleurid’ Peripeltopleurus, from the Middle Triassic (Ladinian, 235–242 Ma) of South China and near the Ladinian/Anisian boundary of southern Switzerland and northern Italy, respectively, represent the most primitive and oldest known thoracopterids. Wushaichthys, the most basal thoracopterid, shows certain derived features of this group in the skull. Peripeltopleurus shows a condition intermediate between Wushaichthys and Thoracopterus in having a slightly asymmetrical caudal fin but still lacking wing-like paired fins. Phylogenetic studies suggest that the evolution of overwater gliding of thoracopterids was gradual in nature; a four-stage adaption following the ‘cranial specialization–asymmetrical caudal fin–enlarged paired fins–scale reduction’ sequence has been recognized in thoracopterid evolution. Moreover, Wushaichthys and Peripeltopleurus bear hooklets on the anal fin of supposed males, resembling those of modern viviparious teleosts. Early thoracopterids probably had evolved a live-bearing reproductive strategy.     

Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes

With about 24,000 extant species, teleosts are the largest group of vertebrates. They constitute more than 99% of the ray-finned fishes (Actinopterygii) that diverged from the lobe-finned fish lineage (Sarcopterygii) about 450 MYA. Although the role of genome duplication in the evolution of vertebrates is now established, its role in structuring the teleost genomes has been controversial. At least two hypotheses have been proposed: a whole-genome duplication in an ancient ray-finned fish and independent gene duplications in different lineages. These hypotheses are, however, based on small data sets and lack adequate statistical and phylogenetic support. In this study, we have made a systematic comparison of the draft genome sequences of Fugu and humans to identify paralogous chromosomal regions ("paralogons") in the Fugu that arose in the ray-finned fish lineage ("fish-specific"). We identified duplicate genes in the Fugu by phylogenetic analyses of the Fugu, human, and invertebrate sequences. Our analyses provide evidence for 425 fish-specific duplicate genes in the Fugu and show that at least 6.6% of the genome is represented by fish-specific paralogons. We estimated the ages of Fugu duplicate genes and paralogons using the molecular clock. Remarkably, the ages of duplicate genes and paralogons are clustered, with a peak around 350 MYA. These data strongly suggest a whole-genome duplication event early during the evolution of ray-finned fishes, probably before the origin of teleosts.     

Reevaluation of the caudal skeleton of some actinopterygian fishes: II. Hiodon,Elops, and Albula

The vertebral centra of Hiodon, Elops, and Albula are direct perichordal ossifications (autocentra) which enclose the arcocentra as in Amia. An inner ring of ovoid cells forms in late ontogeny from the intervertebral space inside the autocentrum. The chordacentrum is reduced or completely absent in centra of adult Elops, whereas it forms an important portion of the centra in adult Hiodon. The posterior portion of the compound ural centrum 3+4+5 is partially (Hiodon) or fully formed by the chordacentrum (Elops, Albula). The haemal arches and hypurals are fused medially by cartilage or bone trabecles of the arcocentrum with the centra, even though they appear autogenous in lateral view in Elops and Albula. The composition of the caudal skeleton of fossil teleosts and the ontogeny of that of Hiodon, Elops, and Albula corroborate a one-to-one relationship of ural centra with these dorsal and ventral elements. The first epural (epural 1) of Elops relates to ural centrum 1, whereas the first epural (epural 2) of Hiodon and Albula relates to ural centrum 2. In Albula, the first ural centrum is formed by ural centrum 2 only. With 4 uroneurals Hiodon has the highest number within recent teleosts. Juvenile specimens of Hiodon have eight, the highest number of hypurals within recent teleosts; this is the primitive condition by comparison with other teleosts and pholidophorids. Reduction of elements in the caudal skeleton is an advanced feature as seen within elopomorphs from Elops to Albula. Such reductions and fusions occur in osteoglossomorphs also, but the lack of epurals and uroneurals separates most osteoglossomorphs (except Hiodon) from all other teleosts.     

An enigmatic actinopterygian (Pisces: Osteichthyes) from the Upper Permian of China

A new actinopterygian fish Yaomoshania minutosquama gen. & sp. nov., from the Upper Permian of the Dzungaria [Junggar] Basin in China is described. The material consists of two very fragmentary specimens showing almost exclusively scale rows. The arrangement of the scale rows of the holotype resembles the reversion lines of acanthodian caudal fins and of cheirolepids. The size and shape of the scales, and the diminishing size of the scales along the rows, is similar to those of acanthodians and those actinopterygians with small scales such as Cheirolepis. However, the histology of the scales demonstrates features that are found in more advanced actinopterygians: superimposed ganoine lamellae, the arrangement of dentine tubules and pulp canals, buried odontodes stacked on each other to make the ornamental ridges, and an asymmetric pattern of growth achieved by extensive remodelling (resorption and redeposition) of all layers of the scale. Yaomoshania minutosquama is proposed as a small-scale bearing, basal actinopterygian, different from Cheirolepis , but characterized by advanced histological characters.     

云南罗平中三叠世翼鳕属一新种及早期辐鳍鱼类系统发育关系（英文）

辐鳍鱼亚纲是现存脊椎动物中最大的类群,包括腕鳍鱼次亚纲、辐鳍鱼次亚纲(包括软骨硬鳞类和新鳍鱼类)和亲缘关系密切的化石类群。已灭绝的翼鳕属(Pteronisculus)是隶属于辐鳍鱼亚纲的一个干群,包括产于马达加斯加、欧洲和北美下三叠统的11个种和中国中三叠统的一个种。根据滇东罗平中三叠世(安尼期)海相地层中发现的5块保存完好的化石,命名翼鳕属一新种,张氏翼鳕(Pteronisculus changae sp. nov.)。这是翼鳕属在中三叠世的第二个确切种,最大体长达295 mm,代表了罗平生物群中已知体型最大的辐鳍鱼亚纲干群物种。新种具有翼鳕属的独特衍征,泪骨具有牙齿,但它又有明显区别于本属其他种的自近裔特征,如间颞骨中部有一个内突起,21根上神经骨,83列侧线鳞。分支分析结果为早期辐鳍鱼类系统发育关系提供了新的见解,认为翼鳕属是Cyranorhis的姐妹群。根据体型和口缘牙齿等特征推测张氏翼鳕是一个快速游动的捕食者,以浮游无脊椎动物和体型较小的鱼类或鱼类幼体为食。作为翼鳕属最年轻的成员之一,张氏翼鳕的发现进一步表明翼鳕的多样性比我们过去认识的要高,古特提斯洋东缘可能是该属在中三叠世早期的避难所。     

Molecular phylogeny of C1 inhibitor depicts two immunoglobulin-like domains fusion in fishes and ray-finned fishes specific intron insertion after separation from zebrafish

C1 inhibitor (C1IN) is a multi-facet serine protease inhibitor in the plasma cascades, inhibiting several proteases, notably, regulates both complement and contact system activation. Despite huge advancements in the understanding of C1IN based on biochemical properties and its roles in the plasma cascades, the phylogenetic history of C1IN remains uncharacterized. To date, there is no comprehensive study illustrating the phylogenetic history of C1IN. Herein, we explored phylogenetic history of C1IN gene in vertebrates. Fishes have C1IN with two immunoglobulin like domains attached in the N-terminal region. The RCL regions of CIIN from fishes and tetrapod genomes have variations at the positions P2 and P1′. Gene structures of C1IN gene from selected ray-finned fishes varied in the Ig domain region with creation of novel intron splitting exon Im2 into Im2a and Im2b. This intron is limited to ray-finned fishes with genome size reduced below 1 Gb. Hence, we suggest that genome compaction and associated double-strand break repairs are behind this intron gain. This study reveals the evolutionary history of C1IN and confirmed that this gene remains the same locus for ∼450 MY in 52 vertebrates analysed, but it is not found in frogs and lampreys.